Limnetica, 32 (2): 269-286 (2013). DOI: 10.23818/limn.32.22 Limnetica, 29 (2): x-xx (2011) c Asociación Ibérica de Limnología, Madrid. Spain. ISSN: 0213-8409
Review of the state of knowledge of crayfish species in the Iberian Peninsula
Iván Vedia∗ and Rafael Miranda
Department of Environmental Biology, University of Navarra, Irunlarrea 1, E-31008 Pamplona, Navarra, Spain.
∗ Corresponding author: [email protected] 2 Received: 22/11/12 Accepted: 21/6/13
ABSTRACT Review of the state of knowledge of crayfish species in the Iberian Peninsula This paper reviews information relevant to managing the four crayfish species present in the Iberian Peninsula. The red swamp crayfish, Procambarus clarkii, signal crayfish, Pacifastacus leniusculus, and Yabbie, Cherax destructor, are classified as invasive alien species by Spanish legislation. The most significant negative impacts of these species in freshwater ecosystems are noted, and some management methods are proposed. In addition, scientific studies addressing the origin and taxonomy of the Iberian white-clawed crayfish, Austropotamobius italicus italicus, are discussed. The Iberian populations of A. i. italicus have been severely diminished since the onset of the expansion of the aphanomycosis disease in 1978. However, this trend began to undergo reversal a few years ago, and the populations of this species are now growing. Finally, current legislation concerning the fishing and conservation of crayfish species is explained and discussed.
Key words: Austropotamobius italicus, Procambarus clarkii, Pacifastacus leniusculus, Cherax destructor, invasive species, aphanomycosis, fishing regulations.
RESUMEN Revisión del estado de conocimiento de las especies de cangrejo de río en la Península Ibérica En este artículo se ha hecho una profunda revisión de toda la información relevante para la gestión de las cuatro especies de cangrejo de río presentes en la Península Ibérica. El cangrejo rojo de las marismas Procambarus clarkii, el cangrejo señal Pacifastacus leniusculus y el cangrejo Yabbie Cherax destructor son consideradas especies exóticas invasoras en la legislación española. Se mencionan los impactos negativos más significativos que estas especies están produciendo sobre los ecosistemas acuáticos y se proponen algunos métodos de gestión. Por otro lado, se exponen los diferentes estudios científicos relacionados con el origen y taxonomía del cangrejo de río que habita en la Península Ibérica (Austropotamobius italicus italicus).Las poblaciones ibéricas de A. i. italicus están muy debilitadas a causa de la enfermedad de la afanomicosis que comenzó a expandirse a partir del año 1978. Aunque esta tendencia cambió hace unos pocos años y las poblaciones están creciendo. Finalmente, se explica y discute la legislación vigente relativa a la conservación y pesca de las especies de cangrejos de río.
Palabras clave: Austropotamobius italicus, Procambarus clarkii, Pacifastacus leniusculus, Cherax destructor, especies inva- soras, afanomicosis, legislación pesquera.
INTRODUCTION lems facing global biodiversity. In fact, invasive alien species are considered the second most sig- The increasing spread of invasive alien species nificant cause of extinctions after habitat destruc- on a global scale is one of the most serious prob- tion (IUCN, 2011). This problem not only affects
14974 Limnetica 32(2), pàgina 269, 21/11/2013 270 Vedia and Miranda biodiversity but also leads to economic, health Peninsula and assess its implications for aquatic and social problems. ecosystem conservation. Aquatic ecosystems are particularly vul- In summary, the principal aim of this paper nerable to the introduction of invasive alien is to analyse the current knowledge regarding species. Fifty percent of the invasive species the conservation status of crayfish conservation present in the Iberian Peninsula are fishes and status in the Iberian Peninsula to develop a better crayfishes. In the inland waters of the Iberian set of scientific criteria with which to implement Peninsula, in particular, there are at least 45 adequate management policies. invasive invertebrate species and 28 invasive vertebrate species (García-Berthou, 2007). Of the 45 invasive species of invertebrates, three are MATERIALS AND METHODS crayfish. These three non-native crayfish species are the red swamp crayfish, Procambarus clarkii, The Iberian Peninsula is a geographically iso- signal crayfish, Pacifastacus leniusculus,and lated area located in southwestern Europe. It is Yabbie, Cherax destructor. surrounded by the Mediterranean Sea and At- Crayfishes are considered keystone species lantic Ocean and is connected to the rest of Eu- because they play an important ecological role rope by the Pyrenees in the northeast. The Iberian in freshwater ecosystems. The influence of these Peninsula covers an approximate surface area of crustaceans on ecosystems is more important 583 254 km2, and it displays an extensive river than might be expected considering their rela- system with 12 main hydrographic basins. tive abundance or total biomass. These species More than 150 scientific articles and 15 books occupy a central position in the food chains were reviewed to evaluate the current state of of many ecosystems, simultaneously acting as knowledge about crayfishes and their ecological both prey and predators (Geiger et al., 2005). role in the Iberian Peninsula. This literature search Crayfishes constitute one component of the was completed using the ISI Web of Knowledge connecting link between aquatic and terrestrial academic database and Google Scholar search ecosystems, facilitating the energy flow between engine. Library resources and printed publica- them (Larson & Olden, 2011). tions available at the Library of Sciences of the In addition, crayfishes play an important University of Navarra were also employed. economic and social role. For example, in some To analyse Iberian and global crayfish stocks areas, such as the Guadalquivir marshes, the and production, the official database and fish- red swamp crayfish represents an important ery statistics of the Food and Agriculture Or- food resource, and its trade provides an extra ganization of the United Nations (FAO, 2012) contribution to the local economy (Cano & Ocete, were consulted. This database includes the vol- 1994). Additionally, recreational crayfish fishing is ume of aquatic species caught by country or area, deeply rooted in local culture (Alonso et al., 2000). by species, by major FAO fishing areas and by The specific goals of this paper are as follows: year for all types of fishing, i.e., commercial, in- 1) to review the current knowledge of crayfishes dustrial, recreational and subsistence. It also in- in the Iberian Peninsula by describing the main cludes aquaculture production and the breeding characteristics of native and alien crayfishes of other types of fish. in terms of their origin, taxonomy, distribution Finally, to analyse the existing legislation range and associated impacts; 2) to analyse and related to crayfish in the Iberian Peninsula, evaluate the ecological function performed by the following sources were consulted: 1) the crayfish in aquatic ecosystems; 3) to note some “Boletín Oficial del Estado” (BOE) (Official commercial, economic and production-related Bulletin of the State), to check whether any of information about crayfish; and 4) to review the the crayfish species are included in the Spanish existing legislation addressing the management Catalogue of Endangered Species or in the Span- of all crayfish species present in the Iberian ish Catalogue of Invasive Alien Species; 2) “El
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Diário da República Portuguesa” (Diary of the fish and mammal species, thus playing a key role Portuguese Republic); and 3) the Bulletins of the in aquatic ecosystems (Zaccara et al., 2004). regional Spanish administrations were checked The phylogeny, taxonomy, biogeography and to obtain information on fishing regulations and origin of A. i. italicus have been discussed at the conservation status of crayfish species in length in recent years (Grandjean et al., 2002). the Iberian Peninsula. The Official Bulletins The purpose of this section is to explain the of Andalucía, Aragón, Asturias, Cantabria, various scientific studies related to this complex Castilla-La Mancha, Castilla y León, Cataluña, topic. Based on traditional taxonomic analyses, Extremadura, Galicia, La Rioja, Madrid, Murcia, scientists temporarily defined a group of species Navarra and the Comunidad Valenciana were and subspecies of this crayfish as a specific consulted for this purpose. In the País Vasco, complex, designated Austropotamobius pallipes where each province exhibit different legisla- s.l. (Chiesa et al., 2011). Mitochondrial 16S tions, the Official Bulletins of Álava, Vizcaya rRNA analysis and morphological studies show and Guipúzcoa were analysed separately. that A. pallipes s.l. can be divided into two different species: 1) A. pallipes, which is present in France, Switzerland, Germany and the British RESULTS Isles, and 2) A. italicus, which is found in Spain, France, Italy, south of the Alps and the Balkans Crayfish species in the Iberian Peninsula (Grandjean et al., 2000; 2002; Zaccara et al., 2004; Fratini et al., 2005; Schulz & Grandjean, Of the three families of crayfish that exist in 2005; Trontelj et al., 2005). The distribution the world (Parastacidae, Cambaridae and Astaci- range of the Iberian white-clawed crayfish dae), only the Astacidae family is native to Eu- differs if we consider this specific complex to rope (Souty-Grosset et al., 2006). The four cray- be separated into one or two species. Figure 1a fish species that live in the Iberian Peninsula shows the global distribution of A. italicus and are described below. A. pallipes (Grandjean et al., 2002; Trontelj et al., 2005; Alonso, 2011). In addition, A. italicus Austropotamobius italicus italicus exhibits a high intraspecific genetic oscillation, (Faxon, 1914) separating it into three (Grandjean et al., 2002) or four (Fratini et al., 2005) subspecies, with A. The white-clawed crayfish, Austropotamobius italicus italicus being the subspecies found in the italicus italicus, is endemic to freshwater Iberian Peninsula (Grandjean et al., 2002; Fratini ecosystems in southwestern Europe (Alonso, et al., 2005). This subspecies is distributed in 2011). Its populations have been substantially Italy, southern Switzerland and Spain (Fratini et reduced during recent decades, mainly because al., 2005). In contrast, figure 1b shows the global of the crayfish plague and other factors such distribution of A. pallipes when it is considered as pollution or habitat alteration (Alonso et al., as a single species in Europe (Souty-Grosset et 2000). However, this trend has changed because al., 2006; Chiesa et al., 2011). A. pallipes and the number of populations has been growing A. italicus present significant differences in their in the last few years (Alonso, 2012). Prior to 16S rRNA mitochondrial genes. Grandjean et al. this decline, A. i. italicus was widely distributed (2002) observed a difference of 3.6-5.4 % be- throughout peninsular freshwater habitats, except tween the two species, and a difference of 3.5 % in the more western areas, the highest mountain was detected by Ghia et al. (2006). Diéguez- ranges and the sub-desert areas of the southeast Uribeondo et al. (2008) and Trontelj et al. (2005) and Ebro River valley (Matallanas et al., 2011). observed mitochondrial DNA variations of 11.3 This species inhabits rivers, streams and reser- % and 7.0 %, respectively. It is estimated that voirs with clean and well-oxygenated waters and 2.75 % variation in the 16S rRNA mitochon- represents the main food source for many bird, drial gene sequence indicates isolation of one
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Figure 1. a) Distribution range of the genus Austropotamobius in Europe according to Grandjean et al. (2002). Black colour indicates the Austropotamobius pallipes distribution range, and grey colour represents the Austropotamobius italicus distribution range. b) The Austropotamobius pallipes distribution range in Europe according to Souty-Grosset et al. (2006). a) Distribución del género Austropotamobius en Europa de acuerdo con Grandjean et al. (2002). El color negro indica el rango de distribución de Austropotamobius pallipes y el color gris representa el rango de distribución de Austropotamobius italicus. b) Rango de distribución de Austropotamobius pallipes en Europa de acuerdo con Souty-Grosset et al. (2006). million years between species. Therefore, these mention of crayfish in the Iberian Peninsula two species could have been isolated over two was made in the Calatayud (Asso, 1784). In the million years ago (Grandjean et al., 2002; Schulz geographical-statistical-historical Dictionary of & Grandjean, 2005). Due to its wider accep- Spain written by Madoz (1845-1850), crayfish tance, the taxonomic hypothesis represented in were cited as a fishery resource in the Ebro basin figure 1a will be employed in the present paper. and in some localities situated in the Duero and The origin of the Iberian populations of the Tajo basins (Maldonado et al., 2008). Moreover, white-clawed crayfish (A. i. italicus) has been none of the main languages spoken in the Iberian widely discussed in the scientific community. Peninsula has a specific vernacular name for Some authors believe that the Iberian popula- crayfishes. They are referred to as “cangrejos tions of A. i. italicus were the result of human de río” (literally “river crabs”) in Spanish, with translocations coming from northwestern Italy similar translations being found in Basque, Cata- in the 17th century. The first molecular studies lan and Galician, or “lagostim” in Portuguese based on mitochondrial data found very low (a generic name for all the species of Astacidea genetic diversity within the Iberian populations group), most likely related to their similarity of A. i. italicus, in addition to shared haplotypes with some types of marine shrimps. and non-significant differentiation between the Other authors consider A. i. italicus to be the Iberian and the Italian subspecies (Grandjean et only native crayfish species in the Iberian Penin- al., 2000; 2002; Fratini et al., 2005; Trontelj et sula (Beroiz et al., 2008; Diéguez-Uribeondo et al., 2005). Moreover, the absence of historical al., 2008; Pedraza-Lara et al., 2010; Matallanas sources and fossil records supports this hypoth- et al., 2011; 2012; Alonso, 2011). Beroiz et al. esis, given the importance of this crustacean in (2008) used RAPD-PCR to show that there was other European cultures. The “Relaciones To- higher genetic variability in Spanish populations pográficas de Felipe II” is an exhaustive record of of the white-clawed crayfish than reported Spanish fisheries and their exploitation that was by previous authors, who employed different registered for all the areas under the king’s man- markers. Mitochondrial analyses also suggest date, but no specific mention of the presence of a possible natural origin for this species as a this crayfish were found in this resource (Miguel consequence of a complex biogeographic and Clavero, pers. comm.; Campos, 2003). The first demographic history and further recent natural
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or human-mediated processes that might have to the first introduction of North American shaped its current genetic structure (Pedraza- crayfishes to Europe (Diéguez-Uribeondo et Lara et al., 2010). Genetic analyses of peninsular al., 1997). The first isolation of A. astaci ob- populations employing nuclear and mitochon- tained from white-clawed crayfish corpses in drial markers (COI and 16S rDNA)haveshown Spain (Burgos and Álava) came from signal similar or even higher genetic diversity com- crayfish. Thus, North American crayfish in- pared to that reported in previous studies on other troductions could have been the route through Spanish and European populations (Matallanas which this disease entered the Iberian Peninsula et al., 2011; 2012). Eight different mitochondrial (Diéguez-Uribeondo et al., 1997). DNA haplotypes have been found in this species, The American crayfishes, Pacifastacus le- and it would be impossible to explain this degree niusculus and Procambarus clarkii,serveas of genetic diversity as having occurred within a vectors of the aphanomycosis pathogen during few hundreds of years (Matallanas et al., 2011). their whole lifespan (Diéguez-Uribeondo et The source of the crayfish plague (aphanomy- al., 1997; Edgerton et al., 2002; ISSG, 2011; cosis) is the water mould Aphanomyces astaci Longshaw, 2011). However, American cray- (Schicora, 1906). This mould is included among fishes are resistant to this disease as a result of the 100 worst invasive species in the world coevolution between the pathogen and host. As (Lowe et al., 2000). This pathogen has decreased a consequence of this coevolution, the pathogen the populations of native European crayfish is restricted exclusively to the cuticle of these species during the past several decades, es- crayfishes, except when they experience stress pecially since the introduction of non-native (Diéguez-Uribeondo et al., 1997; Edgerton et crayfishes infected with the pathogen. However, al., 2002; Longshaw, 2011). other factors such as saprolegniasis, pollution, This pathogen exhibits three different stages: habitat alteration, climatic drought and overfish- the mycelium, zoospore and cyst stages (Oidt- ing also affect white-clawed crayfish populations mann et al., 2002). Many zoospores are formed (Diéguez-Uribeondo et al., 1997; Alonso et al., when an infected crayfish is dying or has recently 2000; Edgerton et al., 2002). died. These zoospores constitute the dispersion The A. i. italicus populations found in Spain structures of the pathogen. They are able to sur- started to decrease dramatically in 1978 (Dié- vive for up to two weeks in the mud, and they guez-Uribeondo et al., 1997). According to are motile in the water for three days at 10 ◦C Alonso et al. (2000), the decline of these crayfish (Edgerton et al., 2002). Nevertheless, it is diffi- populations was more pronounced in the central cult for this pathogen to survive for a long period and southern areas of the Iberian Peninsula. of time in a natural environment in the absence of Between 1990 and 2000, there were an estimated a suitable host. Its spores and mycelium die when 700 remaining populations of white-clawed exposed to extreme temperatures and desiccation crayfish (Alonso et al., 2000). However, this neg- (Oidtmann et al., 2002). Sodium hypochlorite, ative trend showed a change at the beginning of MgCl2, iodine and malachite green can be used this century as a consequence of administrative to sterilise and/or reduce sporulation (Edgerton et restoration plans, and a total of 1086 populations al., 2002), although Oidtmann et al. (2002) sug- were estimated to inhabit this region in 2010 gested that the best decontamination method is to (Alonso, 2011). However, these populations boil materials at 100 ◦C for one minute. remain fragmented and restricted to small river The infection generated by A. astaci can be sections, which are usually isolated from the spread easily from one river basin to another main stream where pathogen-carrying alien through the movements of crayfishes and fishes crayfish are present, and their average individual or when attached to contaminated equipment, size is decreasing. such as nets, boots, clothes and other items (e.g., It is believed that the introduction of apha- Oidtmann et al., 2002). Although it is difficult nomycosis was spatially and temporally linked to determine whether a crayfish is infected,
14974 Limnetica 32(2), pàgina 273, 21/11/2013 274 Vedia and Miranda symptoms such as brown melanisation of the rope occurred in southern Spain. It was intro- exoskeleton or whitening of the tail muscle duced for aquaculture production between 1972 are sometimes observed (Edgerton et al., 2002). and 1974 in the marshes of the Guadalquivir Once the infection has begun, crayfish usually die River and quickly established itself in the wild after one or two weeks (Edgerton et al., 2002). (Barbaresi & Gherardi, 2000; Geiger et al., 2005; The protection status of the white-clawed Souty-Grosset et al., 2006; Holdich et al., 2009). crayfish varies among different entities. This Several years later, P. clarkii colonised other ar- species has been catalogued as endangered in eas of the Iberian Peninsula, such as the Al- the World Red List (IUCN, 2011) since 2010 bufera of Valencia (1978), the Ebro delta, Zamora (it was previously catalogued as vulnerable). In (1979) and Lugo (Alonso et al., 2000). Human Europe, it is included in the Annex II – species translocations and the sale of live specimens at of community interest, meaning that its con- fish markets supported its expansion (Geiger et servation requires the designation of Special al., 2005; Souty-Grosset et al., 2006). P. clarkii Areas of Conservation (SAC) – Annex V of the is currently the most abundant crayfish species in Habitats Directive and Annex III of the Berne the Iberian Peninsula (Alonso et al., 2000; Souty- Convention. In Spain, A. i. italicus is catalogued Grosset et al., 2006), showing especially high as vulnerable in the National Catalogue of abundance in the middle and lower stretches of Endangered Species, and its protection status rivers (Alonso et al., 2000; Oscoz et al., 2008). differs among different regional administrations. Figure 2a shows that most of its European popu- lations are found in the Iberian Peninsula. Procambarus clarkii (Girard, 1852) The ecological characteristics of the red swamp crayfish have triggered a series of nega- The red swamp crayfish, Procambarus clarkii, tive socio-economic, health and environmental is native to the wetlands of the southern United impacts since its introduction to the Iberian States of America (U.S.A.) and northeastern Peninsula (Geiger et al., 2005; Larson & Olden, Mexico (Larson & Olden, 2011). It is the most 2011). Furthermore, its introduction to the lower invasive crayfish species in the world and is Guadalquivir has caused a conflict of interests: found in Africa, Asia, Europe and North and P. clarkii produces high economic losses and is South America (Lowe et al., 2000; Larson & responsible for massive devastation of rice crops, Olden, 2011). The features responsible for the but is also an important source of wealth as a high invasive potential of this species are its high fishing resource (Cano & Ocete, 1994). fecundity, rapid growth, short life cycle, high As noted above, rice crops are severely im- aggressiveness and ability to adapt to poor envi- pacted by the red swamp crayfish. These impacts ronmental conditions (e.g., low oxygen, salinity, are produced indirectly as a consequence of the acidity and pollution) and to tolerate sudden abundant galleries that this species digs within changes in water levels (e.g., Geiger et al., the cultivation areas of this crop, thus damaging 2005). With regard to this last characteristic, it the water drainage capability of these fields is important to note that P. clarkii can withstand (Barbaresi & Gherardi, 2000). In addition, the long periods of drought by excavating galleries red swamp crayfish feeds on rice, reducing the more than 2 m deep to increase its proximity germination and establishment of rice seedlings to the water table, where the humidity is higher (Cano & Ocete, 1994; Souty-Grosset et al., (Barbaresi & Gherardi, 2000; Souty-Grosset et 2006). It also damages various types of infras- al., 2006). In summary, this invasive species can tructure, such as water canals, bridges, roads and survive in a wide range of environmental conditions highways (Cano & Ocete, 1994). and habitats, such as crop areas, lakes, canals, In 1997, a tularemia outbreak occurred in the rivers, marshes and swamps (ISSG, 2011). province of Cuenca in association with P. c l a r k i i The red swamp crayfish is native to Louisiana handling (Díaz de Tuesta et al., 2001).Francisella marshes (U.S.A.), and its first introduction to Eu- tularensis tularensis (McCoy & Chapin, 1912) is
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Figure 2. a) Red swamp crayfish, Procambarus clarkii, b) signal crayfish, Pacifastacus leniusculus, and c) Yabbie, Cherax destructor distribution range in Europe. The signal crayfish distribution range in Norway, Slovakia, Croatia, Estonia and Denmark is not represented on the map; c Scientific publications MNHN, Paris, 2006 (modified from Holdich et al. 2009 for Procambarus clarkii and Pacifastacus leniusculus and from Souty-Grosset et al. 2006 for C. destructor). a) Distribución del cangrejo rojo de las marismas Procambarus clarkii, b) cangrejo señal Pacifastacus leniusculus y c) Yabbie Cherax destructor en Europa. Para Pacifastacus leniusculus la distribución en Noruega, Eslovaquia, Croacia, Estonia y Dinamarca no está representada en el mapa c Publicaciones científicas MNHN, Paris, 2006 (modificado de Holdich et al. 2009 para Procambarus clarkii y Pacifastacus leniusculus y de Souty- Grosset et al. 2006 para C. destructor).
the bacterium that causes this serious infectious suggest that the red swamp crayfish increases disease. This bacterium has been found in the water turbidity, hence reducing light penetration stomach, hepatopancreas and water of P. clarkii, and macrophytic algae productivity (Geiger et but not in its exoskeleton. These findings indicate al., 2005; Larson & Olden, 2011; Marchi et al., that the red swamp crayfish is not a direct trans- 2011). It also modifies biogeochemical cycles mission vector of tularemia, and the most likely and unbalances the food chain, decreasing the cause of this outbreak was the contamination complexity of ecosystems (Marchi et al., 2011). of river water with animals killed by tularemia (lagomorphs), which then also infected P. clarkii. Pacifastacus leniusculus (Dana, 1852) Furthermore, this non-native species gener- ates negative environmental impacts on macro- The signal crayfish, Pacifastacus leniusculus,is phytic algae, amphibians, molluscs and macro- endemic to the northwestern U.S.A. and south- invertebrate diversity in aquatic ecosystems western Canada and inhabits a wide range of (Rodríguez et al., 2005; Souty-Grosset et al., habitats, from small streams to large rivers and 2006; Correia et al., 2005; 2007). Some authors lakes. This species is found in 24 European coun-
14974 Limnetica 32(2), pàgina 275, 21/11/2013 276 Vedia and Miranda tries and is the most widespread alien species in swamp crayfish and the white-clawed crayfish Europe (Souty-Grosset et al., 2006; Holdich et (Cuéllar & Cuéllar, 2000). The signal crayfish al., 2009; Johnsen & Taugbøl, 2010) (Fig. 2b). was thought to represent the perfect “ecological The signal crayfish is better adapted than the red counterpart” of the white-clawed crayfish and swamp crayfish to upstream stretches. This crus- to be resistant to aphanomycosis. Nevertheless, tacean exhibits higher rates of growth and sexual there is no scientific evidence supporting the maturation than the white-clawed crayfish, but actual creation of this “green barrier”, as both lower rates than the red swamp crayfish. Its eco- species, P. clarkii and P. leniusculus, have been logical characteristics include tolerance of salty wa- observed to coexist within the same stretch ter, a wide temperature range, resistance to pH lev- of river without any appreciable difficulties els above six and a high capacity for enduring long (Oscoz et al., 2008; Larson & Olden, 2011). In periods out of water (Souty-Grosset et al., 2006). fact, Alonso & Martínez (2006) studied shelter The signal crayfish was introduced to competition between red swamp crayfish and Spain between 1974 and 1975 at two crayfish signal crayfish under laboratory conditions, and hatcheries, which were located in the Cifuentes in most experiments, the red swamp crayfish was River (Guadalajara) and Ucero River (Soria), both the first species to be observed in a shelter respectively, with the introduced individuals (70.8 %) and the long-term winner (62.5 %). coming from Simmontorp, a Swedish crayfish Additionally, P. leniusculus also carries the hatchery (Alonso et al., 2000). In later years, pathogen responsible for crayfish plague in its new signal crayfish introductions were carried cuticle. The introduction of these non-native out, but with the individuals involved coming crayfish species has further complicated the directly from North America. The restocking situation because they were introduced together programs of some administrations, such as with branchiobdellidan species. The bran- Navarra, País Vasco and Castilla y León, facil- chiobdellidans, or crayfish worms, are obligate itated its expansion (Alonso et al., 2000). By ectosymbionts related to both oligochaetes and 2004, it was present in Orense, Castilla y León, hirudinids (Souty-Grosset et al., 2006). There are Cantabria, País Vasco, Navarra, Teruel, Lleida, seven endemic European species of Branchiob- Castellón, Comunidad Valenciana, Cuenca, dellidae belonging to the genus Branchiobdella. Guadalajara, Albacete, Madrid and Granada. In some river stretches, signal crayfish are The first reference to signal crayfish populations infected by a non-indigenous species of Bran- in southern Spain in the literature comes from chiobdellidae, Xironogiton victoriensis (Gelder 2000, in the Riofrio River (Loja, Granada) (Dana & Hall, 1990) (Oscoz et al., 2010). This species et al., 2010), though its presence in other south- causes a negative impact among fishermen who ern locations has been reported as well. While reject “infected” individuals for consumption. the distribution range of signal crayfish in the The signal crayfish also produces negative ef- Iberian Peninsula is not currently as wide as the fects in macrophytes, macroinvertebrates, sna- distribution of the red swamp crayfish (Fig. 2b), kes, benthic fishes and amphibian larvae (John- its populations are undergoing expansion in the sen & Taugbøl, 2010). central peninsula as a result of illegal translo- cations. The fishing legislations related to this Cherax destructor (Clark, 1936) species have been changing. The initial mode of management was fishing area limitations, The Yabbie, Cherax destructor is native to east- whereas free fishing is currently allowed (An- ern Australia and is found in New South Wales, nex 1, www. limnetica.net/internet). Victoria and South Australia (Souty-Grosset et As mentioned previously, some regional al., 2006). This crustacean inhabits marshes, administrations conducted a signal crayfish streams, rivers and reservoirs with sandy and introduction program in the 1980s with the aim muddy bottoms where the water exhibits a of creating a “green barrier” between the red moderate turbidity level, thus offering better
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protection from predators such as fish and birds Impacts and management of crayfishes (Withnall, 2000). The Yabbie can withstand tem- peratures between 1 ◦C and 35 ◦C, with its opti- The introduction of non-native crayfishes to mum range for growth falling between 20 ◦Cand freshwater ecosystems has provided an important 30 ◦C. When the water temperature drops below food resource for species at higher trophic levels, 16 ◦C, its metabolism decreases to a level corre- such as fish, birds and mammals (Geiger et al., sponding to partial hibernation (Withnall, 2000). 2005). Energy from detritus is transferred directly The first introduction of C. destructor into to higher trophic levels, thereby reducing the Spain and Europe took place in Girona (Cat- number of trophic levels. Consequently, a decline alonia) in 1983, involving specimens from in the importance of macrophyte algae, herbivores California (Souty-Grosset et al., 2006). Sub- and primary carnivores takes place, altering the sequently (1984-1985), another introduction overall structure and function of aquatic food chains was conducted in the province of Zaragoza, (Rodríguez et al., 2005; Geiger et al., 2005). where a population was eventually stabilised in The red swamp crayfish exhibits more herbiv- Gordués, near Sos del Rey Católico (Holdich orous habits than the white-clawed crayfish, thus et al., 2009). Because C. destructor is sensitive producing significant changes in aquatic ecosys- to aphanomycosis, some of its populations tems (Rodríguez et al., 2005). For example, fol- have been eradicated using the crayfish plague lowing the introduction of the red swamp crayfish pathogen. However, some populations persist into Lake Chozas (León), a decline in the popula- to the present day (Holdich et al., 2009). It tions of herbivorous birds (e.g., ducks, coots) was is believed that there are at least four stable observed due to a reduction of food and nesting populations in Spain: one in Aragon and three in habitats (Rodríguez et al., 2005). Navarra (Souty-Grosset et al., 2006) (Fig. 2c). Furthermore, there are studies showing that Moreover, this species has been detected in other non-native crayfishes have threatened and even European countries in recent years. For example, eradicated amphibian species in many rivers and a population was detected in Italy in 2008, and lakes in the Iberian Peninsula (Ilhéu et al., 2007). one individual was reported in Lake Geneva, For example, Rodríguez et al. (2005) found that Switzerland (Scalici et al., 2009). four frog species disappeared after the introduc- The Yabbie is commercially produced in some tion of P. clarkii. regions of Australia (New South Wales, Victoria Nevertheless, the presence of non-native and South Australia), and it is considered a delicacy crayfishes has a positive impact in some cases and sold live in North America, Switzerland, Ger- on certain fish-eating species, such as the otter many and England (Souty-Grosset et al., 2006). Lutra lutra L., the bittern Botarus stellaris L., This species displays highly aggressive, com- the little egret, Egretta garzetta L., and the petitive and predatory behaviour. Similar to the heron Ardea purpurea L. (Barbaresi & Gherardi, American crayfishes (P. clarkii and P. leniuscu- 2000; Correia et al., 2005; Geiger et al., 2005; lus), C. destructor is able to dig a network of tun- Rodríguez et al., 2005). nels with depths of 0.5 m to 2 m to survive dry Eradication methods could become an summer periods (Withnall, 2000). These galleries alternative means of eliminating non-native cray- damage crops, lawns, dams and irrigation canals fishes, although such methods are not always (Gherardi, 2007). effective (Peay & Hiley, 2001). For example, The Yabbie is considered a serious threat to applying heavy fishing pressure could appear to native Cherax tenuimanus populations in west- be a good control mechanism for these popula- ern Australia because of its high reproductive po- tions apriori, although this increased pressure tential and high tolerance to various environmen- may have negative effects because fishermen tal conditions. For these reasons, this invasive often act as dispersal agents (Alonso et al., species is considered a serious threat to European 2000). A total of 25 492 signal crayfishes were aquatic ecosystems (Souty-Grosset et al., 2006). eliminated from the Riofrío (Loja, Granada)
14974 Limnetica 32(2), pàgina 277, 21/11/2013 278 Vedia and Miranda between 2005 and 2008, as shown by the “Plan cation of signal crayfish populations in the UK. Andaluz para el Control de las Especies Exóticas They concluded that the eradication or control Invasoras”. In eliminating these crayfishes, of a signal crayfish population is only likely to workers used a combination of methods, such be achieved through chemical control (biocides). as minnow traps, electrofishing, hand catching Peay et al. (2006) studied a new methodology and artificial shelters. Thus, the size of the signal based on the use of natural pyrethrum for crayfish population and the risk of its dispersion eradicating signal crayfish in ponds. were dramatically minimised, as the popula- For the eradication of C. destructor, Scalici tion was brought near or below the minimum et al. (2009) proposed that direct pathogen ap- size for reproduction. However, other studies plication or the introduction of infected crayfish have suggested that manual removal has not should be implemented. However, these methods effective been at any level of effort (e.g., Peay may represent a high risk to the local popula- & Hiley, 2001). To control non-native crayfish tions of A. i. italicus, which is also susceptible to populations, management decisions should be the disease (Oscoz et al., 2010). Thus, following focused on controlling the main factor involved this procedure to eradicate C. destructor would in their expansion, which is human transloca- only be carried out in areas where no evidence of tions. Nevertheless, other effective methods can the white-clawed crayfish species is found. Al- be applied. Corkum (2004) and Stebbing et al. though low water temperatures constitute natural (2003) have suggested that capturing signal cray- barriers to the spread of this species, there is no fish using pheromones could become a widely way to prevent human translocations, which are applied eradication method in the future because the main means of the spreading of all crayfish pheromones also act as repellents for local species (Scalici et al., 2009). crayfish populations (Johnsen & Taugbøl, 2010). The possibility of isolating and developing a Global and Spanish crayfish production biological control agent specifically to influence invasive species should be considered (Freeman According to FAO statistics, the red swamp cray- et al., 2007). Additionally, the construction of fish has been the species with the highest global dams has proven to be effective in restraining the production since the 1970s (ISSG, 2011; FAO, expansion of P. clarkii to headwaters, thereby 2012). The global production of A. i. italicus and preventing new aphanomycosis infections in A. pallipes during the 1950s, 1960s and 1970s white-clawed crayfish populations (Dana et al., was also remarkable, considering that their range 2011). Peay & Hiley (2001) considered manual was limited to a small region in Europe (Fig. 1). removal, habitat destruction, barriers, predators, For example, an average of 1380t of A. i. itali- diseases, pheromones and biocides for the eradi- cus and A. pallipes was produced annually during
Table 1. Evolution of the average annual production of crayfish species present in the Iberian Peninsula by country (tonnes, t) (FAO 2012). Evolución de la producción promedio anual por países (toneladas, t) de las especies de cangrejo de río presentes en la Península Ibérica (FAO 2012). Country Species 50-59 60-69 70-79 80-89 90-99 00-09 2010
Kenya P. clarkii 49 33 17 20 U.S.A. P. clarkii 16 242 3775 28 663 24 438 33 995 52 942 China P. clarkii 139 726 563 281 Indonesia C. destructor 28 Spain & Italy P. clarkii 59 2533 2263 200 1509 Finland P. leniusculus 1.7 5.8 137 226 A. italicus 1380 440 679 37 Australia C. destructor 5 185 143 51
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the 1950s, compared to 16t of P. clarkii.How- ever, this pattern was dramatically reversed a few years later, when the production of A. i. italicus and A. pallipes decreased dramatically, mainly in response to aphanomycosis disease. In contrast, the production of P. clarkii increased exponen- tially, reaching annual global production of 173 938t (Table 1). In contrast to the red swamp cray- fish, there has historically been little or no global production of P.leniusculus and C. destructor,al- though there has been an increasing trend in the last three decades. Figure 3. Evolution of the annual production (tonnes, t)ofA. i. italicus and P. clarkii in the Iberian Peninsula between the European crayfish production is lower than years 1950 and 2010 (FAO 2012). Evolución de la producción Asian or American production. Nevertheless, anual (toneladas, t)deA. i. italicus y P. clarkii en la Península the crayfish market has been very important to Ibérica entre los años 1950 y 2010 (FAO 2012). the economy of some Spanish regions (Cano & Ocete, 1994; Souty-Grosset et al., 2006) tion of 22t. Subsequently, the annual produc- (Table 1). Until 2002, almost all production data tion of this species increased to 400t in 1980 for P. clarkii came from America (U.S.A.) and, and 5662t in 1991 (Fig. 3). In recent years, red to a lesser extent, from Europe. However, the swamp crayfish production has been estimated to FAO started recording production statistics in be 1500t per year, although this is most likely Asia (China) in 2003, and the global production an underestimation. data were multiplied six times (Table 1). The Ministry of Agriculture, Fisheries and Food There is no other place in America where (2007) reported an index of commercialisation for the red swamp crayfish has as great an impact the red swamp crayfish of 2 or 3 t/year in El on the economy as it has in the southern states. Palmar (Valencia) and more than 6 t/year in Cata- This species is produced and consumed as lonia between 2005 and 2006. Additionally, the food in several areas. The state of Louisiana region of Castilla y León produces a total of 3·105 dominates both aquaculture and wild capture crayfish per year, with a value of 57 660 Euros. fisheries of this crayfish, which contribute over 150 million dollars annually to the state econ- Legislation and commercialisation omy. In Louisiana, approximately 48 000 ha are used to cultivate this crustacean, representing The legislation addressing white-clawed crayfish 90-95 % of U.S. production (McAlain & Ro- conservation is complex because it includes maire, 2007). Nevertheless, China is the largest regulations related to conservation, national- and crayfish producer in the world, with a 2010 total regional-scale commercialisation and fishing production that was ten times higher than that regulations at the provincial level. While many of the U.S.A. (Table 1). of the regional administrations have developed Figure 3 shows a chronology of the annual their own laws for fishing and conservation, production of the white-clawed crayfish and red the marketing of this species is still nationally swamp crayfish in Spain in tonnes (t). Since data regulated. Limitation in live crayfish com- have been available (starting in 1980), A. i. itali- mercialisation is important for the control of cus has shown an annual production of between non-native crayfish populations. Although the 500t and 3000t. However, the production of sale of red swamp crayfish is allowed in Spain, the signal crayfish was only one tonne per year the commercialisation of signal crayfish is not between 1998 and 2002. The first production permitted by national legislation. This prohi- data for the red swamp crayfish in Spain were bition could explain the different patterns of obtained in 1977, indicating an annual produc- dispersion observed for the two species.
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Management and conservation Iberian and Italian populations (Grandjean et al., 2002; Fratini et al., 2005; Trontelj et al., 2005). Table 2 shows the global, Spanish and Portuguese In addition, certain authors believe that there are cataloguing of crayfish species that inhabit the no fossils or historical references available to Iberian Peninsula. Furthermore, it includes the help track the biogeographic evolution of this most important features of each species. Annex 1 species (Madoz, 1845-1850). Nevertheless, there (supplementary material: www.limnetica.net/in- are many reviews that criticise these studies due ternet) summarises the principal laws for these to the small number of samples used (eight pop- species included in the local and national legisla- ulations and only one individual for each one). tion of Spain and Portugal. According to Chiesa et al. (2011), the mitochon- drial gene sequencing method used by most au- Fishing regulations thors to study the phylogeny of the Austropota- mobius genus is not reliable, and they argue that All the information concerning authorisations re- this technique only provides a partial view be- garding fish sizes, numbers of catches and fish- cause it solely reflects the maternal phylogeny. ing periods for the red swamp crayfish and signal Furthermore, these studies did not consider the crayfish is provided within the same Annex. major reduction of population sizes and subse- quent human translocations of Iberian A. i. itali- cus, which could also reduce their genetic diver- DISCUSSION sity, causing a bottleneck (Diéguez-Uribeondo et al., 2008; Pedraza-Lara et al., 2010). In addi- The origin of Iberian A. i. italicus populations tion, new references to the white-clawed cray- has been a topic of debate in recent years. First, fish in the Iberian Peninsula have been found in it is essential to clarify whether A. i. italicus is medieval and Arabic texts (Diéguez-Uribeondo an introduced species or the only native species et al., 2008). The question of vernacular names of crayfish in the Iberian Peninsula, as crayfish complicates the situation but does not prove that management policies should be completely dif- the white-clawed crayfish is introduced. Other re- ferent depending on the answer to this question. cent studies have shown that this species could be Some authors believe that the Iberian populations native to the Iberian Peninsula because the genet- of this species are the result of human translo- ics of its peninsular populations differ sufficiently cations from Italy because mitochondrial data from its Italian populations to infer that their dif- have shown very low genetic diversity between ferentiation occurred more than a few hundreds
Table 2. Summary of crayfish species present in the Iberian Peninsula and catalogued in the world (IUCN), Spain (Real Ordinance 139/2011 and 1628/2011) and Portugal (Ordinance-Law no 49/2005 and Ordinance-Law 565/99). LC: least concern; VU: vulnerable; EN: endangered; S: south; NE: northeast; NW: northwest; E: east. Tabla resumen de las especies de cangrejo de río presentes en la Península Ibérica y su catalogación mundial (IUCN), española (Real Decreto 139/2011 y 1628/2011) y portuguesa (Decreto-Ley no 49/2005 y Decreto-Ley 565/99). LC: preocupación menor; VU: vulnerable; EN: en peligro; S: sur; NE: noreste; NW: noroeste; E: este. A. i. italicus P. clarkii P. leniusculus C. destructor
Origin SW Europe S U.S.A., NE Mexico NW U.S.A. and SW Canada E Australia Family Astacidae Cambaridae Astacidae Parastacidae Year of introduction — 1973-1974 1974-1975 1984-1985 Aphanomycosis Sensitive Resistant (carrier) Resistant (carrier) Sensitive Global legislation EN LC LC VU Spanish legislation VU Invasive Invasive Invasive Portuguese legislation Community interest Invasive Exotic —
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of years ago (Beroiz et al., 2008; Pedraza-Lara et habitat where A. i. italicus could be reintroduced al., 2010; Matallanas et al., 2011; 2012). Thus, and recovered. Some possible eradication meth- these authors suggest that there are no strong ar- ods are mentioned in the management section. guments calling into question the indigenous sta- The negative impacts caused by signal cray- tus of the white-clawed crayfish. fish in freshwater ecosystems are well known There is a long-standing consensus suggesting (Dunn et al., 2009; Johnsen & Taugbøl, 2010). that the main cause for the decline of A. i. itali- However, this species has been subjected to in- cus populations has been the Aphanomyces astaci correct management policies for several years, water mould. The life cycle and dispersal mech- focused on its utilisation and the conservation anisms of Aphanomyces astaci are well known, of its populations as an exploitable resource. It and it is considered to be a pathogen that requires seems logical that all non-native Iberian crayfish a host to survive. Thus, it is important to imple- species, i.e., Procambarus clarkii, Cherax de- ment management measures to account for the structor and Pacifastacus leniusculus, should be fact that non-native crayfishes, specifically Pro- addressed using the same management policies, cambarus clarkii and Pacifastacus leniusculus,are directing all efforts towards their eradication. carriers of the crayfishplague. However, C. destruc- The current knowledge of Iberian C. destruc- tor and A. i. italicus are sensitive to crayfish plague. tor crayfish populations seems to be sparse. Con- The protection status of the white-clawed sidering the aggressive, competitive and preda- crayfish differs among the different regional ad- tory behaviour of this species, its presence and ministrations of Spain. A. i. italicus is catalogued spreading could have negative effects in the fu- as “endangered” in nine regional administrations ture. Thus, the implementation of measures to and “vulnerable” in six regional administrations. prevent its spread is urgently required, despite the In addition, five regional administrations have a fact that its populations are currently very restricted. recovery plan for this species. To reduce these ThedataonSpanishcrayfish production were efforts and considering Spain together with obtained from an official source (FAO), whose Portugal as an ecological unit, it seems logical to accuracy is not high. These data were collected develop a single recovery plan for the species and from the Agriculture Minister through annual make the regional administrations responsible for direct polling of responsible managers in each implementing and applying adequate measures. province and it is known that some provinces Many data suggest that the introduction of the have provided data without conducting any red swamp and signal crayfishes between 1972 control of recreational fishing in the past. For and 1975 was directly related to the beginning of this reason, subsequent interpretation of these the crayfish plague because white-clawed cray- data must be conducted with caution. fish populations began to decline sharply after 1978 (Diéguez-Uribeondo et al., 1997). This is Legislation: conservation and fisheries a clear example of how the introduction of non- native species negatively affects the environment. Analysis of the existing legislation related to Some regional administrations have carried out the conservation and management of Iberian signal crayfish restocking under the following crayfish species yields ambiguous results. The two hypothetical goals: 1) to create a “green bar- Spanish Catalogue of Invasive Alien Species rier” between the red swamp crayfish and the na- (Boletín Oficial del Estado, 2011), as described tive crayfish and 2) to introduce an “ecological in its transitional provision, includes all of substitute” for the white-clawed crayfish. Never- the introduced crayfish species in the Iberian theless, the signal crayfish does not prevent the Peninsula prior to the implementation of Law passage of the red swamp crayfish, and it car- 42/2007 addressing hunting, fishing and forestry. ries the pathogenic crayfish plague agent. The Under this provision, “in order to prevent these current aim is to find a way to eradicate these invasive species from spreading beyond their non-native populations by procuring a potential current range, hunting, fishing and forestry
14974 Limnetica 32(2), pàgina 281, 21/11/2013 282 Vedia and Miranda strategies are proposed as management, control of non-native crayfish populations, 2) strictly and eradication measures”. monitoring watercourses to prevent invasion by This provision also states that if hunting, fish- these or other species of alien crayfishes and 3) ing and forestry activities involving one of the informing and warning the human population, species cited therein are promoting its expan- especially fishermen, about the serious effects sion and establishment outside its current range, that the introduction of non-native crayfishes the General Directorate of the Environment and causes in the environment. Forestry Policies must take appropriate steps to manage this species. There is a large body of literature suggesting ACKNOWLEDGEMENTS that non-native crayfish species have a negative impact on freshwater ecosystems (Geiger et al., We appreciate the improvements in English usage 2005; Rodríguez et al., 2005; Souty-Grosset et made by Ibon Tobes. A preliminary draft of this al., 2006; Ilhéu et al., 2007). Therefore, a pri- paper was revised by Enrique Baquero, Jordi Puig mary management objective should be to erad- and Carolina Santamaría. Iván Vedia benefitted icate introduced species and prevent the estab- from a predoctoral grant from the Asociación lishment of new invasive ones. It must be kept de Amigos-University of Navarra (2011-2012). in mind that once a new species is established in the wild, eradication becomes very challeng- ing because of the complexity of ecosystems and REFERENCES the difficulty of finding a method that only af- fects the target species. Thus, it appears that is ALONSO, F., C. TEMIÑO & J. DIÉGUEZ-URI- quite difficult to eradicate P. clarkii and P. lenius- BEONDO. 2000. Status of the white-clawed cray- culus populations, though it is easier to prevent fish, Austropotamobius pallipes (Lereboullet, 1858), new introductions of non-native species. Some in Spain: distribution and legislation. Bulletin authors suggest that the best way to avoid hu- Français de la Pêche et de la Pisciculture, 356: 31–53. man translocations is through fishing prohibition ALONSO, F. & R. MARTÍNEZ. 2006. Shelter com- to avoid generating expectations related to fish- petition between two invasive crayfish species: a ing. At present, there are few populations of C. laboratory study. Bulletin Français de la Pêche et destructor, and it is very important to prevent the de la Pisciculture, 380–381: 1121–1132. expansion of this species. ALONSO, F. 2011. Austropotamobius italicus (Fa- Fishing regulations for the signal crayfish xon, 1914). In: Atlas y Libro Rojo de los Inver- have been changing during recent years in a tebrados amenazados de España (Especies Vul- manner that differs between the Spanish regional nerables). J. R. Verdú, C. Numa, E. Galante (eds.): administrations. For several years, the fishing 651–672. Dirección General de Medio Natural y regulations published by regional administrations Política Forestal, Ministerio de Medio Ambiente, established limitations such as quotas and sizes Medio rural y Marino, Madrid, Spain. to regulate and preserve the populations of signal ASSO, I. J. 1784. Introductio in Oryctographiam et crayfish. However, the recent policies of most Zoologiam Aragoniae. Accedit. Enumeratio Stir- regional administrations allow fishing of signal pium in eadem Regione noviter detectarum. Fac- crayfish, without any type of restriction. On the simile edition, Amsterdam, Netherlands. BARBARESI, S. & F. GHERARDI. 2000. The inva- other hand, in the regional administrations of sion of the alien crayfish Procambarus clarkii in Andalucía, Castilla-La Mancha, Comunidad Va- Europe, with particular reference to Italy. Biologi- lenciana, Extremadura, Guipúzcoa and Murcia, cal Invasions, 2: 259–264. signal crayfish fishing is forbidden (Annex 1). BEROIZ, B., C. CALLEJAS, F. ALONSO & M. D. In conclusion, to properly manage cray- OCHANDO. 2008. Genetic structure of Spanish fish populations in the Iberian Peninsula, we white-clawed crayfish (Austropotamobius palli- propose the following actions: 1) eradication pes) populations as determined by RAPD analysis:
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